Nicotinic receptor activation contrasts pathophysiological bursting and neurodegeneration evoked by glutamate uptake block on rat hypoglossal motoneurons
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Key points: Impaired uptake of glutamate builds up the extracellular level of this excitatory transmitter to trigger rhythmic neuronal bursting and delayed cell death in the brainstem motor nucleus hypoglossus. This process is the expression of the excitotoxicity that underlies motoneuron degeneration in diseases such as amyotrophic lateral sclerosis affecting bulbar motoneurons. In a model of motoneuron excitotoxicity produced by pharmacological block of glutamate uptake in vitro, rhythmic bursting is suppressed by activation of neuronal nicotinic receptors with their conventional agonist nicotine. Emergence of bursting is facilitated by nicotinic receptor antagonists. Following excitotoxicity, nicotinic receptor activity decreases mitochondrial energy dysfunction, endoplasmic reticulum stress and production of toxic radicals. Globally, these phenomena synergize to provide motoneuron protection. Nicotinic receptors may represent a novel target to contrast pathological overactivity of brainstem motoneurons and therefore to prevent their metabolic distress and death. Excitotoxicity is thought to be one of the early processes in the onset of amyotrophic lateral sclerosis (ALS) because high levels of glutamate have been detected in the cerebrospinal fluid of such patients due to dysfunctional uptake of this transmitter that gradually damages brainstem and spinal motoneurons. To explore potential mechanisms to arrest ALS onset, we used an established in vitro model of rat brainstem slice preparation in which excitotoxicity is induced by the glutamate uptake blocker dl‐threo‐β‐benzyloxyaspartate (TBOA). Because certain brain neurons may be neuroprotected via activation of nicotinic acetylcholine receptors (nAChRs) by nicotine, we investigated if nicotine could arrest excitotoxic damage to highly ALS‐vulnerable hypoglossal motoneurons (HMs). On 50% of patch‐clamped HMs, TBOA induced intense network bursts that were inhibited by 1–10 μ m nicotine, whereas nAChR antagonists facilitated burst emergence in non‐burster cells. Furthermore, nicotine inhibited excitatory transmission and enhanced synaptic inhibition. Strong neuroprotection by nicotine prevented the HM loss observed after 4 h of TBOA exposure. This neuroprotective action was due to suppression of downstream effectors of neurotoxicity such as increased intracellular levels of reactive oxygen species, impaired energy metabolism and upregulated genes involved in endoplasmic reticulum (ER) stress. In addition, HMs surviving TBOA toxicity often expressed UDP‐glucose glycoprotein glucosyltransferase, a key element in repair of misfolded proteins: this phenomenon was absent after nicotine application, indicative of ER stress prevention. Our results suggest nAChRs to be potential targets for inhibiting excitotoxic damage of motoneurons at an early stage of the neurodegenerative process.
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Nicotinamide has recently been investigated to determine its relevance in improving ALS symptoms and thus motor function.
“Nicotinamide has recently been investigated to determine its relevance in improving ALS symptoms and thus motor function (120).”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [120]
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Hong, D., Zhang, C., Wu, W., Lu, X., & Zhang, L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1133546 · Cited by 38 · see citing works
- Authors
- Corsini, S., Tortora, M., & Nistri, A.
- Affiliations
- Scuola Internazionale Superiore di Studi Avanzati (IT)
- Corresponding author
- Nistri, Andrea
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2016-08-03
- Volume
- 594
- Issue
- 22
- Pages
- 6777-6798
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC5108918
- OpenAlex
- W2468656762
- Cited by
- 16
- References
- 129
- Citations by year
- 2025: 2 · 2023: 1 · 2022: 1 · 2021: 3 · 2019: 1 · 2018: 2 · 2017: 4 · 2016: 2
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- SDL (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- nicotinic acetylcholine receptors, excitotoxicity, TBOA, hypoglossal motoneurons, amyotrophic lateral sclerosis, neuronal bursting, neuroprotection, nicotine, endoplasmic reticulum stress, reactive oxygen species, synaptic inhibition, neurodegeneration
- MeSH terms
- Action Potentials, Amyotrophic Lateral Sclerosis, Animals, Aspartic Acid, Brain Stem, Glucosyltransferases, Hypoglossal Nerve, Motor Neurons, Nicotine, Receptors, Nicotinic, Rats, Wistar, Reactive Oxygen Species, Glutamic Acid, Nicotinic Antagonists, Neurodegenerative Diseases, Rats, Endoplasmic Reticulum Stress
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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